Social Cognitive and Affective , 2016, 1–12

doi: 10.1093/scan/nsw106 Original Manuscript

Oxytocin enhances inter- synchrony during social coordination in male adults Yan Mu,1 Chunyan Guo,2 and Shihui Han1

1School of Psychological and Cognitive Sciences, PKU-IDG/McGovern Institute for Brain Research, Beijing Key 2 5 Laboratory of Behavior and Mental Health, Peking University, Beijing, China and Beijing Key Laboratory of Learning and Cognition, Department of Psychology, Capital Normal University, Beijing, China

Correspondence should be addressed to Shihui Han, School of Psychological and Cognitive Sciences, Peking University, Beijing, China. E-mail: [email protected].

Abstract 10 Recent brain imaging research has revealed oxytocin (OT) effects on an individual’s brain activity during social interaction but tells little about whether and how OT modulates the coherence of inter-brain activity related to two individuals’ coord- ination behavior. We developed a new real-time coordination game that required two individuals of a dyad to synchronize with a partner (coordination task) or with a computer (control task) by counting in mind rhythmically. (EEG) was recorded simultaneously from a dyad to examine OT effects on inter-brain synchrony of 15 neural activity during interpersonal coordination. Experiment 1 found that dyads showed smaller interpersonal time lags of counting and greater inter-brain synchrony of alpha-band neural during the coordination (vs control) task and these effects were reliably observed in female but not male dyads. Moreover, the increased alpha-band inter-brain syn- chrony predicted better interpersonal behavioral synchrony across all participants. Experiment 2, using a double blind, placebo-controlled between-subjects design, revealed that intranasal OT vs placebo administration in male dyads improved 20 interpersonal behavioral synchrony in both the coordination and control tasks but specifically enhanced alpha-band inter- brain neural oscillations during the coordination task. Our findings provide first evidence that OT enhances inter-brain syn- chrony in male adults to facilitate social coordination.

Key words: EEG; inter-brain synchrony; neural ; oxytocin; social coordination

25 Introduction 2012), and the processing of stimuli that probe social synchrony The neuropeptide oxytocin (OT) plays a key role in human social (Levy et al., 2016). However, to our knowledge, previous brain 40 interactions by modulating the underlying cognitive and neural imaging studies have focused on OT effects on an individual’s processes (Bartz et al., 2011; Meyer-Lindenberg et al., 2011; brain activity related to social cognition and behavior. Social Hurlemann and Scheele, 2015; Ma et al., 2016). Behavioral re- interactions require at least two to communicate mutu- 30 search has shown that intranasal administration of OT com- ally. This is particularly important for interpersonal coordin- pared to placebo increases social trust (Kosfeld et al., 2005), ation that precedes communication by means of language both 45 enhances interpersonal coordination (Arueti et al., 2013) and evolutionarily and ontogenetically (Semin, 2007) and lays a key motivates ingroup favoritism during cooperation (De Dreu et al., foundation for prosociality and cooperation (Noe,€ 2006; 2010a, 2011; De Dreu and Kret, 2015; Ma et al., 2015). Brain imag- Wiltermuth and Heath, 2009; Reddish et al., 2013). 35 ing research has further revealed that intranasal administration Recent brain imaging research has taken advantage of of OT versus placebo influences social cognition and behavior hyperscanning technique that allows recording brain activity 50 by modulating the neural activity related to trusting behavior from two individuals simultaneously (Montague, 2002) to (Baumgartner et al., 2008), reciprocated cooperation (Rilling et al., examine the functional role of inter-brain activity in social

Received: 16 December 2015; Revised: 13 July 2016; Accepted: 3 August 2016

VC The Author (2016). Published by Oxford University Press. For Permissions, please email: [email protected]

1 2|Social Cognitive and Affective Neuroscience, 2016, Vol. 00, No. 00

interactions (Dumas et al., 2011; Konvalinka and Roepstorff, without any action and thus was not contaminated by syn- 65 2012; Babiloni and Astolfi, 2014). For example, using functional chronous perceptual processing and motor responses. magnetic imaging (fMRI), researchers have localized Experiment 1 aimed to identify the functional role of alpha inter-brain co-activations in the anterior and middle cingulate band inter-brain synchrony in social coordination using the 5 cortices during an economic exchange task (King-Casas et al., real-time coordination game. In addition, because it has been 2005) and found enhanced inter –brain of the assumed that women develop a particular style of interacting 70 inferior frontal activity associated with shared during with other women and are more cooperative with same-sex in- face-to-face communication (Koike et al., 2016). Functional near dividuals compared to men (Maccoby and Jacklin, 1987; infrared spectroscopy (fNIRS) and magnetoencephalographic Maccoby, 1990), Experiment 1 further compared interpersonal 10 (MEG) studies have also revealed enhanced inter-brain coher- behavioral synchrony and inter-brain synchrony in male and fe- ence associated with behavioral coordination during social co- male dyads. A recent social adaptation model of OT function 75 operation (Cui et al., 2012), leader-follower communication posits that the multifaceted role of OT in socio-affective proc- (Jiang et al., 2015) and joint hand-action tasks (Zhdanov et al., esses is to improve the capability for social adaptation and the 2015). Electroencephalography (EEG) has also been used to OT function is more significant in less socially adapted individ- 15 examine dynamic inter-brain oscillatory activities with high uals (Ma et al., 2016). If inter-brain synchrony plays a role in so- time resolution (i.e. millisecond) (Dumas et al., 2010; Astolfi cial adaptation, we would then expect greater OT effects on 80 et al., 2012; Yun et al., 2012). Particularly related to the current inter-brain synchrony in the subject group who show less inter- work, it has been shown that inter-brain synchrony in the alpha personal behavioral synchrony. Because Experiment 1 found band (8–12 Hz) activity emerged and correlated with behavioral that female relative to male dyads showed better interpersonal 20 interactional synchrony (Dumas et al., 2010). The alpha band behavioral synchrony and greater alpha band inter-brain syn- inter-brain synchrony also occurred when two pilots coordi- chrony, Experiment 2 further investigated OT effects on inter- 85 nated with each other during simulating takeoff and landing brain synchrony during the coordination tasks in male partici- (Astolfi et al., 2012), suggesting that the alpha band inter-brain pants using a double blind, placebo-controlled between-sub- synchrony can be used as a neural marker of interpersonal jects design. Of particular interest was whether interpersonal 25 coordination. synchronous performance and inter-brain synchrony in male While the previous hyperscanning research has shown subjects could be improved by intranasal administration of OT 90 increasing evidence for a key role of inter-brain synchrony in compared to placebo. Findings of improved interpersonal coord- social coordination, the molecular mechanism involved in ination and inter-brain synchrony in male subjects due to OT inter-brain synchrony remains unknown. Given the previous (vs placebo) treatment would provide insight into the neurobio- 30 findings of OT effects on brain activity involved in interacting logical mechanism of synchronized brain activity during social behavior and the functional significance of inter-brain syn- coordination. 95 chrony in social interactions, we hypothesized that OT is engaged in synchronization of neural activities of two brains during social coordination. Because the previous studies that Materials and methods 35 examined inter-brain (Dumas et al., 2010; Astolfi et al., 2012) and Participants intra-brain (Tognoli et al., 2007) activity have shown consistent evidence for the involvement of alpha-band activity in social co- Experiment 1 recruited 68 healthy Chinese adults, including 17 ordination, we further predicted that OT would enhance the male dyads (mean age 6 SD ¼ 22 6 2 years) and 17 female dyads inter-brain phase synchrony of alpha-band neural oscillations (mean age 6 SD ¼ 22 6 2 years). There was no age difference 100 40 during coordination behavior. between male and female groups (t(66) ¼ 1.13, P ¼ 0.26). Our hypothesis was tested using a novel combination of Experiment 2 recruited 60 male Chinese adults with 15 dyads hyperscanning-EEG setup, OT (vs placebo) treatment and a new randomly assigned to OT treatment and 15 dyads to placebo real-time coordination game (Figure 1). The real-time coordin- treatment (mean age 6 SD ¼ 22 6 2 vs 23 6 3 years). There was ation game was designed for testing social coordination in no age difference between OT and placebo groups (t(58) ¼0.85, 105 45 which two participants (or a dyad) were instructed to count in P ¼ 0.40). All participants were recruited by online advertise- mind with a 1-s rhythm for 6–10 s and to synchronize with each ment and were randomly paired so that two participants of a other in order to make a button press at the same time after dyad had not known each before their participation and had no counting (Figure 1A).The coordination task was compared with discussion of strategy for the coordination game. All partici- a control task, which required counting to coordinate with a pants were right-handed, had normal or corrected-to-normal 110 50 computer clock, to control influences of cognitive/affective vision, reported no abnormal neurological history and were processes related to counting, social and motor re- paid for their participation. Informed consent was obtained sponses. Feedback regarding a dyad’s synchronizing perform- prior to the study. This study was approved by a local ethics ance was given after counting on each trial so as to motivate committee. participants for coordination with a partner and to help them to 55 differentiate between coordination with a partner and syn- chronization with a computer. The behavioral performance and Stimuli and procedure 115 EEG activity were recorded simultaneously from a dyad via EEG was recorded simultaneously from a dyad during the coord- using a dual-EEG system (Figure 1B). This dual-EEG setup is ination and control tasks in Experiment 1. Two individuals of suited for assessing interpersonal behavioral performance and each dyad were seated in a sound-shielded room and separated 60 inter-brain EEG activity and for testing the association between by two monitors. All participants wore headphones to block interpersonal behavioral synchrony (by calculating response sounds of their button press. This setup blocked both visual and 120 time lags) and inter-brain synchrony (by calculating phase syn- auditory signals that might deliver messages between two indi- chrony of continuous alpha-band activity) in a dyad. The inter- viduals of a dyad. Stimuli were simultaneously presented to brain synchrony was estimated when a dyad viewed a fixation two participants of each dyad on two identical monitors and Y. Mu et al | 3

Fig. 1. Illustration of the design and EEG recording setup. (A) During EEG recording, each block of 10 trials started with a 3-s task instruction. On each trial a number was presented for 500 ms to indicate the time in second for counting in mind. Participants began to count in mind while looking at the fixation until they finished counting and pressed a button. Feedback bars were then presented for 1 s. During the coordination task, participants were asked to coordinate with their partners so as to respond simultaneously. During the control task, participants were asked to coordinate with the clock of a computer so as to count as accurately as possible. A red/ green bar with numbers on a feedback screen indicated the performance of each participant in the coordination task and a white bar indicated the time recorded by a computer in the baseline task. The length of each bar represented the relative duration of participants’ counting. (B) The setup for EEG recording. EEG was recorded from a dyad simultaneously and continuously using two 32-channel EEG systems. Stimuli were simultaneously presented to two individuals of a dyad on two monitors connected to the same server.

their responses were recorded using two identical keyboards. counterbalanced across participants. All the stimuli were cre- 25 Both the monitors and keyboards were connected to the same ated and displayed using the Matlab PsychoToolbox (Brainard, server computer. This setup enabled to compare interpersonal 1997; Pelli, 1997). To promote participants’ motivation for syn- behavioral synchrony and inter-brain EEG activity (Figure 1B). chronization, they were given a credit for each successful syn- 5 On each trial a dyad were presented with an integer (from 6 to chronous response (i.e. an interval less than 300 ms between 10) for 500 ms that indicated time in seconds. Participants were the responses of a dyad or between the responses of a partici- 30 asked to start counting in minds once the integer was replaced pant and a computer) and their payments for participation were by a fixation. Participants were asked to synchronize with his/ calculated based on the credits they obtained. Prior to the EEG her partner (the coordination task) or with a computer (the con- recording, participants were given 20 trials for practice. There 10 trol task) during counting in order to press a button simultan- were eight sessions of EEG recording. Each session consisted of eously using the left/right index finger with a partner or with a two blocks of 10 trials. The order of the coordination and control 35 computer when finishing counting (Figure 1). The coordination tasks was counterbalanced over sessions so that half sessions and control tasks were indicated by the color (yellow or blue) of started with the coordination task and half with the control a disk on which an integer was displayed. On each trial, after a task. 15 delay of 1500–2500 ms following participants’ responses, feed- A double-blind, placebo-controlled between-subjects design back on their performances was displayed on each monitor sim- was used in Experiment 2. The stimuli and procedures in 40 ultaneously. A red and a green bar with numbers assigned to Experiment 2 were the same as those in Experiment 1 except each participant were presented for 1000 ms to indicate their that 15 dyads were randomly treated with OT and 15 dyads with performances in the coordination task. A white bar with ‘*’ indi- placebo 40 min before EEG recording. Each participant was ad- 20 cated the time recorded by a computer in the control task. The ministered with 24 IU OT or placebo (containing all of the active length of each bar represented the relative duration of a partici- ingredients except for the neuropeptide) with intranasal sprays 45 pant’s counting and such intuitionistic information helped par- (three times of four IU into each nostril), similar to the previous ticipants to adjust their counting speed. The assignments of work (Shamay-Tsoory et al., 2009; Hurlemann et al., 2010; Ma different colors to instructions and feedback bars were et al., 2015). Before OT or placebo treatment, participants 4|Social Cognitive and Affective Neuroscience, 2016, Vol. 00, No. 00

completed the Self-Construal Scale(Singelis, 1994) and sampling rate of 250 Hz and stored for off-line analysis. During Interpersonal Reactivity Index (Davis, 1983) to assess their cul- the off-line analysis, EEG was treated with band-pass filtering tural orientations (i.e., independent/interdependent self- (0.1–45 Hz) and re-referenced to the algebraic average of the construals) and empathy ability. electrodes at the left and right mastoids. Regression-based ap- 55 proach was used for artifact rejection. The ocular channel was used to estimate the parameters of ocular artifacts which were 5 Analysis of behavioral performance removed from continuous EEG signal for each participant. To quantify synchronous behavior of each dyad, we calculated EEG during each trial was segmented from 200 to 6000 ms several indices of participants’ performances during the coord- after the onset of number presentation. The 6000 ms was set as 60 ination and control tasks in Experiments 1 and 2. First, the over- the cut off for segmentation because the range of counting time all mean interpersonal synchrony performance of each dyad (6–10 s) is equal or longer than 6 s. After segmentation, the 10 was quantified by calculating the interpersonal time lag: inter-brain phase synchrony index (phase-locking value, PLV) were quantified based on a decomposition of the signal dinter i ¼jðRTi;sub 1 RTi;sub 2Þj=ðRTi;sub 1 þ RTi;sub 2Þ between 8 and 13 Hz in 1 Hz steps, similar to previous studies 65 (Linkenkaer-Hansen et al., 2001; Mu et al., 2008; Mu and Han, where RTi,sub_1 and RTi,sub_2 are reaction times of two individ- 2010; 2013). The signal was then convoluted by the complex th uals of a dyad on the i trial. A smaller dinter_i reflects better Morlet wavelet w (t, f0) (Kronland-Martinet et al., 1987) with a synchrony of a dyad’s responses during counting in mind. Gaussian shape in time (SD rt) and (SD rf) domains

Then, to further assess the probability distributions of highly around its central frequency f0 in the following way: 70 synchronous behavior of each dyad, we applied a normal kernel 2 2 15 function to compute probability density estimate of time lags ðt =2r Þ 2ipf0t wðt; f0Þ¼Ae t e between a dyad’s behavioral responses using n (n ¼ 100) equally

spaced points, x1, ..., xn that cover the whole range of the data with rf ¼ 1/2prt. were normalized so that their total (x). The kernel density estimator at the point x is defined as: energyffiffiffi was 1. The normalization factor A was equal to: p 1=2 ðrt pÞ . Convolution of the signal by a family of wavelets pro- Xn 1 fðxÞ¼ K ðx x Þ vided a time frequency (TF) representation of the signal. A n h i i¼1 wavelet family is characterized by the number of cycles of wavelets (NCW). Here, to acquire better temporal and frequency 75

Where xi is an independent and identically distributed sample resolution, we used slowly ascending NCWs which provide bet- drawn from a distribution with an estimated probability density ter temporal resolution at low and better frequency

20 ƒ. Kh is the kernel function and h (> 0) is a smoothing parameter resolution at high frequencies, similar to the previous of the bandwidth. The probability densities were estimated in studies(Delorme and Makeig, 2004). From the resulting TF pres- MATLAB using these parameters (Gaussian kernel, band- entation of signal, we respectively obtained the estimates of in- 80 width ¼ 1.15). The probability density in each two-spaced points stantaneous power and phase. For statistical analyses, the was compared between the coordination and control tasks in power was first normalized by conversion to a decibel scale, 25 Experiment 1 and between OT and placebo groups in which allowed a direct comparison of effects across frequency Experiment 2. Higher probability density of trials with smaller bands(Pfurtscheller and Aranibar, 1979) and then divided into time lags between a dyad’s behavioral responses manifests bet- six consecutive 1000-ms time intervals. The ANOVAs of alpha 85 ter synchronous behavior. spectral power were conducted on each electrode to test Task The behavioral measures of interpersonal coordination were effect (Coordination vs Counting Tasks) in Experiment1 and to 30 subjected to repeated measures analyses of variance (ANOVAs) test the effects of Task and Treatment (OT vs Placebo) and Task with Task (Coordination vs Control Tasks) as a within-subjects x Treatment interactions in Experiment 2. independent variable in Experiment1 and with Task Similar to the previous studies (Lachaux et al., 1999; Gross 90 (Coordination vs Control Tasks) as a within-subjects independ- et al., 2004; Lutz et al., 2004; Doesburg et al., 2008), we used the ent variable and Treatment (OT vs Placebo) as a between- same Morlet wavelet transform to estimate the inter-brain 35 subjects variable in Experiment 2. Post hoc independent sample phase synchrony in the alpha band. The phase-locking value t tests on behavioral measures were conducted to test sex (PLV) defined as the absolute value of the sum of the phase dif- differences on behavioral performance of each task in ferences of two electrodes (j, k) at time t and frequency f across 95 Experiment 1. N epochs was calculated as: X 1 i½Uj ðf;tÞUk ðf ;tÞ Dual-EEG data acquisition and analysis PLVj;k;t ¼ N j e j N 40 EEG was recorded from a dyad simultaneously and continu- ously during the coordination and control tasks using two 32- PLV is a value between 0 and 1, where 0 indicates randomly channel Neuroscan systems that received synchronizing trig- dispersed phases among all trials and 1 indicates fully phase gers from a parallel port of a server computer (Figure 1B). EEG locked oscillations between electrodes j and k in a specific time 100 was recorded from 30 electrodes arranged according to the window. Inter-brain phase synchrony was estimated by exam- 45 international 10/20 system and referenced to the electrode at ining two electrodes from two individuals of a dyad. We se- the right mastoid. The electrode impedance was kept less than lected 12 representative electrodes from each individual over 5 kohms. Eye blinks and vertical eye movements were moni- the frontal (F3, F4, Fz), central (C3, C4, Cz), parietal (P3, P4, Pz), tored using two electrodes located above and below the left eye. and occipital (O1, O2, Oz) regions for the inter-brain phase syn- 105 The horizontal electro-oculogram was recorded from two elec- chrony analysis, resulting in 144 (12 12) electrode pairs. 50 trodes placed 1.5 cm lateral to the left and right external canthi. The modulations of inter-brain PLV were assessed using EEG was amplified (band pass 0.01–100 Hz), digitized at a ANOVAs with Task as a within-subjects independent variable in Y. Mu et al | 5

Experiment1 and with Task as a within-subjects independent interpersonal behavioral synchrony and inter-brain synchrony variable and Treatment (OT vs Placebo) as a between-subjects of alpha-band activity occurred in two individuals of a dyad variable in Experiment 2. The Greenhouse and Geisser correc- who tried to coordinate with each other but not in two individ- tion was applied to ANOVAs with more than one degree of free- uals of a randomly created dyad (see Supplementary Figure S1). 65 5 dom, and a significance level of alpha ¼ 0.05 was used for all The results indicate that the coordination task itself was unable comparisons (Greenhouse and Geisser, 1959). In addition, to to induce increased inter-brain synchrony between two individ- avoid multiple comparison problems, all the EEG results re- uals from different dyads. ported in our paper were corrected using cluster-based correc- Next we examined whether the degree of inter-brain syn- tion. Clusters were defined by any three adjacent data points chrony was able to predict synchronous behavioral perform- 70 10 (each point covered 100 ms) and any three adjacent electrodes ances across dyads. We conducted a correlation analysis of the pairs. We only reported results from electrode pairs in the clus- mean differential interpersonal time lags (coordination vs con- ters that exceeded the cluster-level threshold (P < 0.05). Pearson trol tasks) and the mean differential alpha band PLVs (coordin- correlation coefficients were computed to evaluate the relation- ation vs control tasks) between the central/posterior electrodes ship between behavior performance and inter-brain neural of one participant and the posterior electrodes of his/her part- 75 15 activity. ner at 4000–5000 ms. This analysis, after excluding one dyad as an outlier whose behavioral performances exceeded two stand- ard deviations from the mean, confirmed that the mean PLV Results was negatively correlated with the differential interpersonal time lag (r(33) ¼0.59, P < 0.001, Figure 2E) and positively 80 Inter-brain synchrony associated with interpersonal correlated with probability density across all dyads (r(33) ¼ 0.47, coordination P < 0.01, Figure 2F). These results indicate that the increased To identify inter-brain neural oscillations related to interper- alpha-band inter-brain synchrony predicted more highly syn- 20 sonal coordination, we first analyzed the mean interpersonal chronous behavioral performances during the coordination (vs time lag between two individuals of each dyad in Experiment 1 control) task and thus provides a potential neural marker of so- 85 in the coordination and control tasks, respectively. We pre- cial coordination. dicted that the motivation to coordinate with a partner can in- crease interpersonal behavioral synchrony in a dyad during the Gender differences in interpersonal coordination and 25 coordination than control tasks. Indeed, the analysis of partici- inter-brain synchrony pants’ behavioral performance across female and male dyads revealed a smaller mean interpersonal time lag (3.21 vs 3.52%, To examine gender differences in interpersonal coordination, F(1,33) ¼ 9.12, P < 0.005, Figure 2A) in the coordination than con- we conducted independent sample t-tests to compare the be- 90 trol tasks. We further examined whether the smaller mean havioral measures between female and male dyads in 30 interpersonal time lag was due to the variation of distribution of Experiment 1. The results of the mean interpersonal time lag of trials with smaller interpersonal time lags in the two tasks by the coordination task was significantly smaller in female than calculating the probability density of interpersonal time lags. male dyads (2.97 vs 3.45%, t(32) ¼2.05, P < 0.05). In line with This analysis confirmed a higher proportion of small interper- this, the probability density of small interpersonal time lags 95 sonal time lags (<4%) (15.3 vs 14.3%, (F(1,33) ¼ 7.37, P < 0.01, (< 4%) was greater in female than male dyads (16.30 vs 14.22%, 35 Figure 2B) in the coordination than control tasks. These results t(32) ¼ 2.41, P < 0.05, Figure 3A). However, there was no signifi- indicated that the motivation to coordinate with a partner cant difference in these behavioral indexes of interpersonal co- (compared to a computer) promoted synchronized counting in ordination in the control task between female and male dyads mind and gave rise to better interpersonal behavioral (mean interpersonal time lag: 3.30 vs 3.74%, t(32) ¼1.46, 100 synchrony. P ¼ 0.15; probability density of small interpersonal time lags: 40 Inter-brain synchrony during the coordination and control 14.99 vs 13.51%, t(32) ¼ 1.59, P ¼ 0.12, Figure 3B). These results tasks was assessed by calculating the inter-brain phase-locking- suggested better interpersonal coordination in female than value (PLV) that reflects the phase synchrony of inter-brain male dyads. activities from two individuals of a dyad. The inter-brain PLV Interestingly, the analysis of EEG data further revealed sig- 105 analysis focused on alpha band activity because the previous nificant gender differences in alpha band inter-brain synchrony 45 work reported increased alpha band inter-brain synchrony dur- between male and female dyads. Specially, female compared to ing interpersonal coordination (Astolfi et al., 2012). The ANOVAs male dyads exhibited stronger task effects on the inter-brain of PLVs revealed significantly greater PLVs of alpha-band activ- synchrony of alpha band activity between the posterior elec- ity between the central electrodes of one participant and the trodes from two individuals of a dyad at 4000–5000 ms 110 posterior electrodes of his/her partner at 4000–5000 ms during (F(1,32)¼ 5.49 to 9.04, ps < 0.05, Figure 4A. Post hoc analyses fur- 50 the coordination than control tasks (F(1,33) ¼ 4.17–7.41, ther confirmed that female relative to male dyads exhibited ps < 0.05, Figure 2C and D, Supplementary Table S1). stronger inter-brain synchrony of alpha band activity during the To further verify that the increased inter-brain synchrony coordination task (t(32) ¼ 2.17 to 3.11, ps < 0.05) but weaker was specific to two participants who constituted a dyad for co- alpha band inter-brain synchrony in the control task (t(32) ¼ 115 ordination, we conducted a bootstrap analysis to examine 2.11 to 3.17, ps < 0.05). Figure 4B illustrates the electrodes 55 whether the increased interpersonal behavioral and inter-brain that showed increased interbrain alpha band synchrony in fe- synchrony in the coordination (vs counting) task occurred in male than male dyads during the coordination task. any two individuals who did not constitute a dyad for coordin- ation but performed similar counting tasks. Two participants Improved interpersonal coordination by OT from different dyads were randomly selected to create a new 60 dyad sample and their interpersonal behavioral synchrony and Because Experiment 1 showed evidence that male compared to 120 inter-brain synchrony were calculated. We found that the female dyads showed less interpersonal coordination and 6|Social Cognitive and Affective Neuroscience, 2016, Vol. 00, No. 00

Fig. 2. Behavioral and EEG results of Experiment 1. (A) The mean interpersonal time lags during the coordination and control tasks. (B) The probability density estima- tion of interpersonal time lags during the coordination and control task. (C) The electrode pairs that showed enhanced alpha-band inter-brain PLVs in the coordination vs control tasks. These were evident mainly between the central/posterior electrodes of one participant and the posterior electrodes of his/her partner at 4000– 5000 ms. (D) The mean inter-brain PLV between the central/posterior electrodes of one participant and the posterior electrodes of his/her partner at 4000–5000 ms dur- ing the coordination than control tasks. (E) The negative correlation between differential interpersonal time lag and differential alpha-band inter-brain PLV in the co- ordination and control tasks. (F) The positive correlation between differential probability density and differential alpha-band inter-brain PLV in the coordination and control tasks. *P < 0.05, **P < 0.01, ***P < 0.001.

weaker inter-brain synchrony during the coordination task, interpersonal synchrony during the coordination relative to Experiment 2 recruited only male dyads to examine potential control tasks across treatment groups. Moreover, there was a 20 OT effects on interpersonal coordination and inter-brain syn- significant effect of Treatment on the two behavioral indexes of chrony. In Experiment 2, each male dyad were randomly as- coordination (mean interpersonal time lag: F(1, 28) ¼ 10.18, 5 signed to one of the two treatment conditions (OT or placebo) P < 0.005; probability density of small interpersonal time lag: F(1, and were then instructed to perform the coordination and con- 28) ¼ 11.36, P < 0.002, see Figure 5A and B), indicating that OT trol tasks that were identical to those in Experiment 1. EEG sig- treatment improved interpersonal synchronous performances. 25 nals were recorded simultaneously from two participants of a However, OT effects on behavioral synchrony did not differ be- dyad. We first tested whether OT vs placebo treatment facili- tween two tasks (mean interpersonal time lag: F(1, 28) ¼ 0.96, 10 tated interpersonal synchrony by calculating interpersonal time P ¼ 0.34; probability density of small interpersonal time lag: F(1, lags in the coordination and control tasks, respectively. 2 (Task: 28) ¼ 0.01, P ¼ 0.94), suggesting that OT promotes behavioral coordination vs control tasks) x 2 (Treatment: OT vs placebo) synchronous performance regardless of type of partner (person 30 ANOVAs of behavioral performance showed significant main ef- vs computer). Because the previous research suggested that OT fect of Task on the mean interpersonal time lag (coordination vs effects on both brain (Liu et al., 2013) and behavioral (Pfundmair 15 control tasks: 3.12 vs 3.41%, F(1, 28) ¼ 11.32, P < 0.005) and the et al., 2014) responses varied across individuals with different probability density of smaller time lags (coordination vs control personal traits, we collected measures of self-construals and tasks: 15.0 vs 14.2%, F(1, 28) ¼ 6.57, P < 0.05). These results repli- empathy traits from participants in Experiment 2 before EEG re- 35 cated the findings of Experiment 1 and suggested better cording. These measures did not differ between placebo and OT Y. Mu et al | 7

Fig. 3. Gender differences in behavioral performances in Experiment 1. (A) The mean value (left panel) of interpersonal time lags and the probability density estimation (right panel) of female and male dyads during the coordination task. (B) The mean value (left panel) of interpersonal time lags and the probability density estimation (right panel) of female and male dyads during the counting task.

Fig. 4. Gender differences in interbrain activity in Experiment 1. (A) Gender differences in the alpha band inter-brain phase synchrony at 4000–5000 ms. The mean val- ues of inter-brain PLV over the central/posterior electrodes in each condition are illustrated for female and male dyads, respectively. (B) The electrodes showing increased alpha band inter-brain synchrony in female than male dyads during the coordination task.

groups (ps > 0.05, see Supplementary Table S2), indicating that the OT and placebo groups, respectively. ANOVAs of the PLVs 15 the group differences in interpersonal coordination in with Task (coordination vs control tasks) as a within-subjects Experiment 2 cannot be attributed to group differences in per- variable and Treatment (OT vs placebo) as a between-subjects sonal traits. To examine dynamic change of behavioral syn- variable revealed greater PLVs of alpha-band activity at 4000- 5 chrony and OT effects over time, we conducted a growth 6000 ms between the posterior regions of the two brains of coefficient modeling (RCM) analysis to assess whether OT a dyad during the coordination than control tasks (F(1,28) ¼ 20 modulations on interpersonal time lag changed over time. The 4.19–9.15, ps < 0.05, Figure 5C, Supplementary Table S4), indi- RCM results showed evidence for decreased interpersonal time cating increased alpha band inter-brain synchrony when coor- lag over time, whereas the OT effect on interpersonal coordin- dinating with a partner compared to a computer. Moreover, 10 ation failed to change over time (see supplementary Results and relative to the control task, the coordination task showed Table S3 for details). stronger OT effects on the inter-brain synchrony of alpha- 25 band activity at 1000–3000 ms between the central region of one participant and the posterior regions of his partner Improved inter-brain synchrony by OT (F(1,28) ¼ 5.39–9.88, ps < 0.05, Figure 5D, Supplementary Table To examine OT effects on inter-brain synchrony during inter- S5). Post hoc analyses confirmed that OT vs placebo treat- personal coordination, we calculated the alpha-band PLVs in ments increased inter-brain synchrony of alpha-band 30 8|Social Cognitive and Affective Neuroscience, 2016, Vol. 00, No. 00

Fig. 5. Behavioral and EEG results of Experiment 2. (A) The mean interpersonal time lags of the OT and placebo groups during the coordination and control tasks. (B) The probability density estimation of interpersonal time lags of OT and placebo groups during the coordination task and control tasks. (C) The electrode pairs that showed enhanced alpha-band inter-brain PLVs at 4000–6000 ms in the coordination (vs control) task. These were evident mainly between the posterior regions of the two brains of a dyad. (D) The electrode pairs that showed significant Task (Coordination, Control) x Treatment (Placebo, OT) interaction at 1000–3000 ms. These were evident mainly between the central/posterior electrodes of one participant and the posterior electrodes of his/her partner. (E) The mean alpha-band inter-brain PLV between central and posterior electrodes at 1000–3000 ms of OT and placebo groups. There were significant OT effects during the coordination but not control tasks. F) The electrodes that showed increased alpha-band inter-brain PLVs by OT (vs placebo) treatment during the coordination task. *P < 0.05, **P < 0.01, ***P < 0.001.

oscillations at 1000–3000 ms during the coordination task alpha-band activity emerged within a time window (e.g., 4000– (ps < 0.05) but not during the control task (ps > 0.05, Figure 5E 5000 ms) close to behavioral responses rather than immediately and F, Supplementary Table S5). after participants started to count in mind. These EEG results were mainly due to the effect of intention of coordination be- cause any processes related to , timing and motor re- 25 Discussion sponses were comparable in the coordination and control tasks. 5 The current study investigated the functional role of inter-brain The inter-brain synchrony observed in our work occurred later synchrony in social coordination based on simultaneous count- than that observed during face-to-face imitation of hand move- ing in mind in two individuals and the potential function of OT ment (Dumas et al., 2010). It seemed that some time was in inter-brain synchrony. Experiment 1 revealed increased required for adjusting the phase of neural oscillations in order 30 interpersonal behavioral synchrony, as indexed by smaller to reach inter-brain synchrony when participants were unable 10 interpersonal time lags of behavioral responses, when a partici- to see/hear each other but tried to coordinate with each other in pant coordinated with a partner than with a computer. This mind. A consisting of the supplementary motor finding provided evidence that the motivation to coordinate area, basal ganglia and cerebellum is activated during interval with each other can improve a dyad’s synchronous responses timing (Buhusi and Meck, 2005). The parietal cortex and visual 35 even when no visual or aural cues were available to guide their cortex are also engaged in event timing (Coull et al., 2004; Zhou 15 coordination. In addition, dyads showed enhanced inter-brain et al., 2014). Consistent with these findings, the inter-brain syn- synchrony of alpha-band neural oscillations (indexed by larger chrony of alpha-band neural oscillations in our work took place inter-brain PLVs) when coordinating with a partner compared between the central/posterior electrodes in a dyad. Previous re- with a computer. Furthermore, the degree of alpha-band inter- search has reported inter-brain synchrony of neural synchron- 40 brain synchrony positively predicted synchronous behavioral ization in a wide range of frequency bands depending on the 20 performances across dyads. The inter-brain synchrony of tasks participants performed (Astolfi et al., 2010; Dumas et al., Y. Mu et al | 9

2010). The task in our study required counting in mind with a synchronization with a partner (compared to a computer). In 65 low frequency (i.e., in a 1-s step) and this may be why the coord- consistent with the better behavioral synchrony, female dyads ination task enhanced the inter-brain synchrony in the alpha- also showed enhanced inter-brain synchrony of alpha-band band activity. neural oscillations relative to male dyads. The results are con- 5 Most interestingly, our findings provided the first neurosci- sistent with a sociocultural perspective that emphasizes the ence evidence that OT is engaged in inter-brain synchrony during role of ontogenetic experiences and assumes that women sur- 70 social coordination. Experiment 2 first showed that intranasal ad- pass men during cooperation with same-sex individuals ministration of OT vs placebo significantly reduced interpersonal (Maccoby and Jacklin, 1987; Maccoby, 1990). It has been reported time lags and increased the number of highly synchronous re- that OT, as a peptide hormone of which the plasma level is 10 sponses during the coordination task in male dyads. In addition, higher in female than male animals (Kramer et al., 2004) and the the effect of OT on interpersonal time lags was sustained over serum level increases after social interaction in women but not 75 time. These results indicate that OT can improve behavioral syn- in men (Miller et al., 2009). Thus one may speculate that the chrony even when dyads were unable to receive any visual or higher plasma level of OT may contribute to the greater inter- aural cues (e.g., body movement and verbal instruction) from brain oscillatory synchronization and facilitate interpersonal 15 each other and reinforces the previous findings of OT-related im- synchrony in females. Female advantages in behavioral and its provement of behavioral coordination (Astolfi et al., 2010; Arueti neural synchrony mechanism provide further insight into mo- 80 et al., 2013). Experiment 2 also showed that OT increased behav- lecular mechanisms of synchronized mind and brain activity. ioral synchrony in the control task. Recent research has shown Several theoretical frameworks have been proposed to ac- that OT can increase people’s tendency to anthropomorphize a count for OT effects on human cognition and behavior. The sali- 20 non-social agent (Scheele et al., 2015). It is likely that participants ence account argues that OT regulates the salience of social under OT treatment may attribute social meaning to a computer cues through its interaction with cognitive (e.g., attention) and 85 so as to treat it like a person. Alternatively, OT may generally in- neural (e.g., the dopaminergic) systems (Shamay-Tsoory and crease participants’ motivation for good performance during their Abu-Akel, 2015). Other accounts emphasizes that OT enhances participation. Most interestingly, Experiment 2 showed evidence affiliative prosocial behaviors (Zak et al., 2007), attenuates stress 25 that OT compared to placebo treatment significantly enhanced during social interaction (McCarthy et al., 1996) and regulates co- inter-brain synchrony of alpha-band activity in the coordination operation and conflict among individuals in the context of 90 task. Unlike the EEG results in Experiment 1, the increased alpha- intergroup relations (De Dreu et al., 2010a; 2010b). The OT effects band inter-brain synchrony in the coordination vs control tasks on the inter-brain synchrony observed in the current study in Experiment 2 was evident at 1000–3000 ms after participants occurred when no social cue was presented (i.e., participants 30 had started to count in mind. This result suggests that OT com- only viewed a fixation cross) and participants did not engage pared to placebo treatment modulated the brain activity associ- any interacting behavior or intergroup interactions, and thus 95 ated with interpersonal coordination by shifting inter-brain cannot be reconciled with these theoretical frameworks. synchrony to an earlier and wider time window. Although OT However, our EEG findings can be understood within a recent treatment reduced the interpersonal time lags during the control social adaptation model of OT function that argues that the fun- 35 task, the related inter-brain synchrony was not affected by OT damental function of OT is to promote social adaptation by treatment. Thus the OT effect on inter-brain synchrony was spe- modulating mental processes and adjusting behaviors during 100 cific to the coordination task during which two participants of a social interactions (Ma et al., 2016). Alpha-band oscillations have dyad intended to coordinate with each other by counting in been suggested to be related to the understanding of others’ mind. mental states, emotion and behavior (Muthukumaraswamy and 40 Previous brain imaging studies have uncovered OT effects Johnson, 2004; Oberman et al., 2005; Oberman et al., 2008).Thus on neural responses related to trusting behavior (Baumgartner the enhanced alpha-band inter-brain synchrony by OT observed 105 et al., 2008), reciprocated cooperation (Rilling et al., 2012) and so- in the current study may reflect a consequence of motivation to cial synchrony (Levy et al., 2016). These studies focused on OT understand other mental states so as to coordinate with others effects on intra-brain activity related to social behavior but did well, suggesting a fundamental neurobiological mechanism for 45 not clarify OT effects on inter-brain activity involved in social social adaption. interactions. Our findings that OT enhanced alpha-band inter- The current work has several limitations which should be ad- 110 brain neural activity that covaried with and predicted interper- dressed in future research. For example, the current work tested sonal behavioral synchrony suggest an OT-related neurobio- OT effects on inter-brain synchrony during coordination only in logical mechanism that helps to couple two agents’ minds and male participants. Because previous studies have shown evi- 50 may mediates the OT improvement effects on interpersonal dence for distinct OT effects on neural underpinnings of social (Arueti et al., 2013) and social cooperation cognitive/affective processes in male and female participants 115 (De Dreu et al., 2010a). Behavioral synchrony has novel affective (Kirsch et al., 2005; Domes et al., 2010; Ditzen et al., 2012), future re- and social consequences regarding cooperation such that move- search should integrate EEG recording and intranasal administra- ment synchrony is associated with stronger feelings of rapport tion of OT to clarify whether OT increases or decreases inter- 55 (Bernieri, 1988) and belonging to a social unit (Lakens, 2010). brain synchrony during coordination in female participants. People who synchronize with others relative to controls showed Second, the small sample size in our work limited the statistical 120 a greater tendency to cooperate with others in group economic power of EEG data analysis. The alpha band PLV did not differ sig- exercises (Wiltermuth and Heath, 2009) and more compassion nificantly between the coordination and control tasks in male and altruistic behavior (Valdesolo and Desteno, 2011). Our EEG participants. Thus it is unknown whether the task modulation of 60 findings suggest a new intermedial neural mechanism (e.g., the alpha band inter-brain synchrony can be observed in a large inter-brain synchrony) by which OT influences interpersonal sample. Moreover, although the OT effect on inter-brain syn- 125 coordination and social cooperation. chrony during coordination was observed in our sample, this Our results in Experiment 1 showed evidence for better should also be confirmed in a large sample. Third, the spatial behavioral synchrony in female than male dyads when resolution of EEG makes it difficult to localize the brain regions 10 | Social Cognitive and Affective Neuroscience, 2016, Vol. 00, No. 00

involved in the coordination task employed in our work. Future Baumgartner, T., Heinrichs, M., Vonlanthen, A., Fischbacher, U., research calls for integration of different imaging techniques (e.g. Fehr, E. (2008). Oxytocin shapes the neural circuitry of trust hyperscanning fMRI-EEG) to identify the neural circuit that is sen- and trust adaptation in humans. , 58, 639–50. sitive to OT effects during the social coordination task. Finally, as Bernieri, F.J. (1988). Coordinated movement and rapport in 60 5 pointed out by Burgess (2013), the alpha band results are more teacher-student interactions. Journal of Nonverbal Behavior, 12, likely to be challenged by spurious coupling. To avoid this, our 120–38. study included the control task which was identical to the coord- Brainard, D.H. (1997). The psychophysics toolbox. Spatial Vision, ination task except that participants had to synchronize with a 10, 433–6. computer. 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Science, 328, 1408–11. This work was supported by the National Natural Science De Dreu, C.K.W., Greer, L.L., Van Kleef, G.A., Shalvi, S., Foundation of China (Projects 31421003, 31470986, Handgraaf, M.J.J. (2011). Oxytocin promotes human ethnocen- 85 91332125), the Ministry of Education of China (Project trism. Proceedings of the National Academy of Sciences USA, 108, 20130001110049), and the Chinese Postdoctoral Science 1262–6. 30 Foundation (Project 2011M500171, 2012T50006). We thank De Dreu, C.K.W., Kret, M.E. (2015). Oxytocin conditions inter- Man Xie, Chao Lang, Bingfeng Li, and Yi Liu for helping with group relations through upregulated in-group empathy, co- EEG data collection and OT/placebo administration. We also operation, conformity, and defense. Biological Psychiatry, 79, 90 thank Ernst Poeppel, Mingzhou Ding, and Michele Gelfand 165–73. for helpful comments on an early draft of this paper. Delorme, A., Makeig, S. (2004). 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